Impact of probiotics and β-glucan on the detoxification and gastrointestinal bioaccessibility ofaflatoxin B1 in a cereal-based fermented beverage (boza)
Main Article Content
Keywords
aflatoxin B1, β-glucan, boza, in vitro digestion, Lactobacillus leichmannii, Saccharomyces boulardii
Abstract
The aim of this study was to investigate the effects of Lactobacillus leichmannii as a probiotic bacteria, Saccharomyces boulardii as a yeast, and β-glucan as a prebiotic on the binding ability of aflatoxin B1 (AFB1) and its bioaccessibility in a cereal-based fermented beverage. For this purpose, nine study groups with their combinations were formed. The amount of unbound AFB1 was determined by high performance liquid chromatography (HPLC) after incubation and during the stomach, small intestine, and colon stages using an in vitro digestion model. After incubation, the highest percentage of AFB1 binding (27.79%) was obtained with S. boulardii. The lowest bioaccessibility was observed with L. leichmannii + S. boulardii at the stomach stage (41%), L. leichmannii + β-glucan at the small intestine stage (52%), and L. leichmannii + S. boulardii + β-glucan at the colon stage (35%). These findings suggest that probiotics and prebiotics reduce aflatoxin bioaccessibility, thereby limiting gastrointestinal absorption.
References
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Chaharaein, M., Sadeghi, E., Mohammadi, R., Rouhi, M., & Soltani, M. (2021). The effect of β-glucan and inulin on the reduction of aflatoxin B1 level and assessment of textural and sensory properties in chicken sausages. Current Research in Food Science, 4, 765–772. https://doi.org/10.1016/j.crfs.2021.10.007
Corassin, C. H., Bovo, F., Rosim, R. E., & Oliveira, C. A. F. d. (2013). Efficiency of Saccharomyces cerevisiae and lactic acid bacteria strains to bind aflatoxin M1 in UHT skim milk. Food Control, 31(1), 80–83. https://doi.org/10.1016/j.foodcont.2012.09.033
Gölünük, S. B., Öztaşan, N., Sözen, H., & Koca, H. B. (2017). Effects of traditional fermented beverages on some blood parameters in aerobic exercises. Biomedical Research, 28, 9475–9480.
Hamad, G. M., Zahran, E., & Hafez, E. E. (2017). The efficacy of bacterial and yeasts strains and their combination to bind aflatoxin B1 and B2 in artificially contaminated infants food. Journal of Food Safety, 37(4), e12365. https://doi.org/10.1111/jfs.12365
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Martinez, M. P., Magnoli, A. P., Pereyra, M. G., & Cavaglieri, L. (2019). Probiotic bacteria and yeasts adsorb aflatoxin M1 in milk and degrade it to less toxic AFM1-metabolites. Toxicon, 172, 1–7. https://doi.org/10.1016/j.toxicon.2019.10.001
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Namaumbo, S., Monjerezi, M., Gama, A., Mlangeni, A. T., Chiutsi‐Phiri, G., & Matumba, L. (2023). Reduction of aflatoxins during brewing of a Malawian maize‐based non‐alcoholic beverage, thobwa. Food Science & Nutrition, 11(6), 2864–2871. https://doi.org/10.1002/fsn3.3266
Papillo, V. A., Vitaglione, P., Graziani, G., Gokmen, V., & Fogliano, V. (2014). Release of antioxidant capacity from five plant foods during a multistep enzymatic digestion protocol. Journal of Agricultural and Food Chemistry, 62(18), 4119–4126. https://doi.org/10.1021/jf500695a
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Pourmohammadi, K., Sohrabi, M., Hashemi, S. M. B., & Amiri, M. J. (2021). A kinetic analysis of the aflatoxin detoxification potential of lactic acid bacteria in Terxine (a cereal-based food). FEMS Microbiology Letters, 368(16), fnab104. https://doi.org/10.1093/femsle/fnab104
Ray, R. C., & Montet, D. (2017). Traditional cereal beverage boza: Fermentation technology, microbial content and healthy effects. In Fermented foods, Part II: Technological interventions. CRC Press. https://doi.org/10.1201/9781315205359
Romero-Sánchez, I., Alonso-Núñez, I., Gracia-Lor, E., & Madrid-Albarrán, Y. (2024). Analysis and evaluation of in vitro bioaccessibility of aflatoxins B1, B2, G1 and G2 in plant-based milks. Food Chemistry, 460, 140538. https://doi.org/10.1016/j.foodchem.2024.140538
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Sarlak, Z., Rouhi, M., Mohammadi, R., Khaksar, R., Mortazavian, A. M., Sohrabvandi, S., & Garavand, F. (2017). Probiotic biological strategies to decontaminate aflatoxin M1 in a traditional Iranian fermented milk drink (Doogh). Food Control, 71, 152–159. https://doi.org/10.1016/j.foodcont.2016.06.037
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Sevim, S., Macit, A., Sancak, B., & Kizil, M. (2024). Aflatoxin M1 mitigation by novel biological agents and evaluation of bioaccessibility with enzymatic digestion in milk. Food Bioscience, 59, 103998. https://doi.org/10.1016/j.fbio.2024.103998
Sevim, S., Topal, G. G., Tengilimoglu-Metin, M. M., Sancak, B., & Kizil, M. (2019). Effects of inulin and lactic acid bacteria strains on aflatoxin M1 detoxification in yoghurt. Food Control, 100, 235–239. https://doi.org/10.1016/j.foodcont.2019.01.028
Tabatabaei-Moradi, L., Sharifan, A., Hajizadeh, K., & Bakhoda, H. (2024). In vitro bioaccessibility, cytotoxicity against liver cells and degradation modeling of aflatoxin B1 in bread by cold atmospheric pressure plasma. Food and Bioprocess Technology, 18, 1405–1416. https://doi.org/10.1007/s11947-024-03532-8
Tajik, H., & Sayadi, M. (2022). Effects of probiotic bacteria of Lactobacillus acidophilus and Lactobacillus casei on aflatoxin B1 detoxification within a simulated gastrointestinal tract model. Toxin Reviews, 41(1), 92–99. https://doi.org/10.1080/15569543.2020.1843180
Tian, M., Zhang, G., Ding, S., Jiang, Y., Jiang, B., Ren, D., & Chen, P. (2022). Lactobacillus plantarum T3 as an adsorbent of aflatoxin B1 effectively mitigates the toxic effects on mice. Food Bioscience, 49, 101984. https://doi.org/10.1016/j.fbio.2022.101984
Udomkun, P., Wiredu, A. N., Nagle, M., Müller, J., Vanlauwe, B., & Bandyopadhyay, R. (2017). Innovative technologies to manage aflatoxins in foods and feeds and the profitability of application–A review. Food Control, 76, 127–138. https://doi.org/10.1016/j.foodcont.2017.01.008
Vasconcelos, R. A. M., Kalschne, D. L., Wochner, K. F., Moreira, M. C. C., Becker-Algeri, T. A., Centenaro, A. I., Colla, E., Rodrigues, P. C. A., & Drunkler, D. A. (2020). Feasibility of L. plantarum and prebiotics on aflatoxin B1 detoxification in cow milk. Food Science and Technology, 41, 627–632. https://doi.org/10.1590/fst.34120
Versantvoort, C. H., Oomen, A. G., Van de Kamp, E., Rompelberg, C. J., & Sips, A. J. (2005). Applicability of an in vitro digestion model in assessing the bioaccessibility of mycotoxins from food. Food and Chemical Toxicology, 43(1), 31–40. https://doi.org/10.1016/j.fct.2004.08.007
Wacoo, A. P., Mukisa, I. M., Meeme, R., Byakika, S., Wendiro, D., Sybesma, W., & Kort, R. (2019). Probiotic enrichment and reduction of aflatoxins in a traditional African maize-based fermented food. Nutrients, 11(2), 265. https://doi.org/10.3390/nu11020265
Wang, X., You, J., Li, X., Xu, Y., Li, Z., & Wang, L. (2025). Polysaccharides: A natural solution for mycotoxin mitigation and removal. Food Chemistry, 496, 146909. https://doi.org/10.1016/j.foodchem.2025.146909
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Arici, M., & Daglioglu, O. (2002). Boza: A lactic acid fermented cereal beverage as a traditional Turkish food. Food Reviews International, 18(1), 39–48. https://doi.org/10.1081/FRI-120003416
Basyigit Kilic, G., & Akpinar Kankaya, D. (2016). Assessment of technological characteristics of non-fat yoghurt manufactured with prebiotics and probiotic strains. Journal of Food Science and Technology, 53, 864–871. https://doi.org/10.1007/s13197-015-2055-1
Borcakli, M., Ozturk, T., & Yesilada, E. (2018). Cereal source and microbial consortia of the starter culture influence the chemical composition and physicochemical characteristics of boza. Turkish Journal of Agriculture and Forestry, 42(6), 412–422. https://doi.org/10.3906/tar-1802-3
Cao, W., Yu, P., Yang, K., & Cao, D. (2022). Aflatoxin B1: Metabolism, toxicology, and its involvement in oxidative stress and cancer development. Toxicology Mechanisms and Methods, 32(6), 395–419. https://doi.org/10.1080/15376516.2021.2021339
Chaharaein, M., Sadeghi, E., Mohammadi, R., Rouhi, M., & Soltani, M. (2021). The effect of β-glucan and inulin on the reduction of aflatoxin B1 level and assessment of textural and sensory properties in chicken sausages. Current Research in Food Science, 4, 765–772. https://doi.org/10.1016/j.crfs.2021.10.007
Corassin, C. H., Bovo, F., Rosim, R. E., & Oliveira, C. A. F. d. (2013). Efficiency of Saccharomyces cerevisiae and lactic acid bacteria strains to bind aflatoxin M1 in UHT skim milk. Food Control, 31(1), 80–83. https://doi.org/10.1016/j.foodcont.2012.09.033
Gölünük, S. B., Öztaşan, N., Sözen, H., & Koca, H. B. (2017). Effects of traditional fermented beverages on some blood parameters in aerobic exercises. Biomedical Research, 28, 9475–9480.
Hamad, G. M., Zahran, E., & Hafez, E. E. (2017). The efficacy of bacterial and yeasts strains and their combination to bind aflatoxin B1 and B2 in artificially contaminated infants food. Journal of Food Safety, 37(4), e12365. https://doi.org/10.1111/jfs.12365
IARC. (2002). IARC (International Agency for Research on Cancer) monograph on the evaluation of carcinogenic risk to humans (Vol. 82, p. 171). International Agency for Research on Cancer—World Health Organization.
Ishikawa, A. T., Hirooka, E. Y., Alvares e Silva, P. L., Bracarense, A. P. F. R. L., Flaiban, K. K. M. d. C., Akagi, C. Y., Kawamura, O., Costa, M. C. d., & Itano, E. N. (2017). Impact of a single oral acute dose of aflatoxin B1 on liver function/cytokines and the lymphoproliferative response in C57Bl/6 mice. Toxins, 9(11), 374. https://doi.org/10.3390/toxins9110374
Ismail, A., Gonçalves, B. L., de Neeff, D. V., Ponzilacqua, B., Coppa, C. F., Hintzsche, H., Sajid, M., Cruz, A. G., Corassin, C. H., & Oliveira, C. A. (2018). Aflatoxin in foodstuffs: Occurrence and recent advances in decontamination. Food Research International, 113, 74–85. https://doi.org/10.1016/j.foodres.2018.06.067
Kabak, B., Brandon, E. F., Var, I., Blokland, M., & Sips, A. J. (2009). Effects of probiotic bacteria on the bioaccessibility of aflatoxin B1 and ochratoxin A using an in vitro digestion model under fed conditions. Journal of Environmental Science and Health, Part B, 44(5), 472–480. https://doi.org/10.1080/03601230902935154
Kabak, B., & Ozbey, F. (2012). Assessment of the bioaccessibility of aflatoxins from various food matrices using an in vitro digestion model, and the efficacy of probiotic bacteria in reducing bioaccessibility. Journal of Food Composition and Analysis, 27(1), 21–31. https://doi.org/10.1016/j.jfca.2012.04.006
Khadivi, R., Razavilar, V., Anvar, S., & Akbari-Adergani, B. (2020). Aflatoxin M1-binding ability of selected lactic acid bacteria strains and Saccharomyces boulardii in the experimentally contaminated milk treated with some biophysical factors. Archives of Razi Institute, 75(1), 63–73.
Kurtuldu, O., & Ozcan, T. (2018). Effect of β‐glucan on the properties of probiotic set yoghurt with Bifidobacterium animalis subsp. lactis strain Bb‐12. International Journal of Dairy Technology, 71, 157–166. https://doi.org/10.1111/1471-0307.12414
Macit, A., Sevim, S., & Kizil, M. (2024). Aflatoxin B1 and M1 detoxification in foodstuffs: Examining the efficacy of probiotics with and without prebiotics–A systematic review. Food Bioscience, 103724. https://doi.org/10.1016/j.fbio.2024.103724
Martinez, M. P., Magnoli, A. P., Pereyra, M. G., & Cavaglieri, L. (2019). Probiotic bacteria and yeasts adsorb aflatoxin M1 in milk and degrade it to less toxic AFM1-metabolites. Toxicon, 172, 1–7. https://doi.org/10.1016/j.toxicon.2019.10.001
Mostafa, S., Damla, D. H., & Mozhgan, E. (2024). Effects of wheat bulgur, maize flour and starch on fermentative characteristics of boza. The Annals of the University Dunarea de Jos of Galati. Fascicle VI – Food Technology, 48(2), 165–173. https://doi.org/10.35219/foodtechnology.2024.2.11
Namaumbo, S., Monjerezi, M., Gama, A., Mlangeni, A. T., Chiutsi‐Phiri, G., & Matumba, L. (2023). Reduction of aflatoxins during brewing of a Malawian maize‐based non‐alcoholic beverage, thobwa. Food Science & Nutrition, 11(6), 2864–2871. https://doi.org/10.1002/fsn3.3266
Papillo, V. A., Vitaglione, P., Graziani, G., Gokmen, V., & Fogliano, V. (2014). Release of antioxidant capacity from five plant foods during a multistep enzymatic digestion protocol. Journal of Agricultural and Food Chemistry, 62(18), 4119–4126. https://doi.org/10.1021/jf500695a
Pereyra, C. M., Gil, S., Cristofolini, A., Bonci, M., Makita, M., Monge, M. d. P., Montenegro, M. A., & Cavaglieri, L. R. (2018). The production of yeast cell wall using an agroindustrial waste influences the wall thickness and is implicated on the aflatoxinB1 adsorption process. Food Research International, 111, 306–313. https://doi.org/10.1016/j.foodres.2018.05.026
Pourmohammadi, K., Sohrabi, M., Hashemi, S. M. B., & Amiri, M. J. (2021). A kinetic analysis of the aflatoxin detoxification potential of lactic acid bacteria in Terxine (a cereal-based food). FEMS Microbiology Letters, 368(16), fnab104. https://doi.org/10.1093/femsle/fnab104
Ray, R. C., & Montet, D. (2017). Traditional cereal beverage boza: Fermentation technology, microbial content and healthy effects. In Fermented foods, Part II: Technological interventions. CRC Press. https://doi.org/10.1201/9781315205359
Romero-Sánchez, I., Alonso-Núñez, I., Gracia-Lor, E., & Madrid-Albarrán, Y. (2024). Analysis and evaluation of in vitro bioaccessibility of aflatoxins B1, B2, G1 and G2 in plant-based milks. Food Chemistry, 460, 140538. https://doi.org/10.1016/j.foodchem.2024.140538
Rosburg, V., Boylston, T., & White, P. (2010). Viability of Bifidobacteria strains in yogurt with added oat beta‐glucan and corn starch during cold storage. Journal of Food Science, 75(5), C439–C444. https://doi.org/10.1111/j.1750-3841.2010.01620.x
Sahebghalam, H., Mohamadi Sani, A., & Mehraban, M. (2018). Assessing the ability of Saccharomyces cerevisiae to bind aflatoxin B₁ from contaminated medium. Journal of Food Safety, 38(5), e12443. https://doi.org/10.1111/jfs.12443
Saladino, F., Posarelli, E., Luz, C., Luciano, F., Rodriguez-Estrada, M., Mañes, J., & Meca, G. (2018). Influence of probiotic microorganisms on aflatoxins B1 and B2 bioaccessibility evaluated with a simulated gastrointestinal digestion. Journal of Food Composition and Analysis, 68, 128–132. https://doi.org/10.1016/j.jfca.2017.01.010
Sarlak, Z., Rouhi, M., Mohammadi, R., Khaksar, R., Mortazavian, A. M., Sohrabvandi, S., & Garavand, F. (2017). Probiotic biological strategies to decontaminate aflatoxin M1 in a traditional Iranian fermented milk drink (Doogh). Food Control, 71, 152–159. https://doi.org/10.1016/j.foodcont.2016.06.037
Serrano-Niño, J., Cavazos-Garduño, A., Cantú-Cornelio, F., González-Córdova, A., Vallejo-Córdoba, B., Hernández-Mendoza, A., & García, H. (2015). In vitro reduced availability of aflatoxin B1 and acrylamide by bonding interactions with teichoic acids from Lactobacillus strains. LWT – Food Science and Technology, 64(2), 1334–1341. https://doi.org/10.1016/j.lwt.2015.07.015
Serrano-Niño, J. C., Cavazos-Garduño, A., Hernández-Mendoza, A., Applegate, B., Ferruzzi, M. G., San Martín-González, M. F., & García, H. S. (2013). Assessment of probiotic strains ability to reduce the bioaccessibility of aflatoxin M1 in artificially contaminated milk using an in vitro digestive model. Food Control, 31(1), 202–207. https://doi.org/10.1016/j.foodcont.2012.09.023
Sevim, S., Macit, A., Sancak, B., & Kizil, M. (2024). Aflatoxin M1 mitigation by novel biological agents and evaluation of bioaccessibility with enzymatic digestion in milk. Food Bioscience, 59, 103998. https://doi.org/10.1016/j.fbio.2024.103998
Sevim, S., Topal, G. G., Tengilimoglu-Metin, M. M., Sancak, B., & Kizil, M. (2019). Effects of inulin and lactic acid bacteria strains on aflatoxin M1 detoxification in yoghurt. Food Control, 100, 235–239. https://doi.org/10.1016/j.foodcont.2019.01.028
Tabatabaei-Moradi, L., Sharifan, A., Hajizadeh, K., & Bakhoda, H. (2024). In vitro bioaccessibility, cytotoxicity against liver cells and degradation modeling of aflatoxin B1 in bread by cold atmospheric pressure plasma. Food and Bioprocess Technology, 18, 1405–1416. https://doi.org/10.1007/s11947-024-03532-8
Tajik, H., & Sayadi, M. (2022). Effects of probiotic bacteria of Lactobacillus acidophilus and Lactobacillus casei on aflatoxin B1 detoxification within a simulated gastrointestinal tract model. Toxin Reviews, 41(1), 92–99. https://doi.org/10.1080/15569543.2020.1843180
Tian, M., Zhang, G., Ding, S., Jiang, Y., Jiang, B., Ren, D., & Chen, P. (2022). Lactobacillus plantarum T3 as an adsorbent of aflatoxin B1 effectively mitigates the toxic effects on mice. Food Bioscience, 49, 101984. https://doi.org/10.1016/j.fbio.2022.101984
Udomkun, P., Wiredu, A. N., Nagle, M., Müller, J., Vanlauwe, B., & Bandyopadhyay, R. (2017). Innovative technologies to manage aflatoxins in foods and feeds and the profitability of application–A review. Food Control, 76, 127–138. https://doi.org/10.1016/j.foodcont.2017.01.008
Vasconcelos, R. A. M., Kalschne, D. L., Wochner, K. F., Moreira, M. C. C., Becker-Algeri, T. A., Centenaro, A. I., Colla, E., Rodrigues, P. C. A., & Drunkler, D. A. (2020). Feasibility of L. plantarum and prebiotics on aflatoxin B1 detoxification in cow milk. Food Science and Technology, 41, 627–632. https://doi.org/10.1590/fst.34120
Versantvoort, C. H., Oomen, A. G., Van de Kamp, E., Rompelberg, C. J., & Sips, A. J. (2005). Applicability of an in vitro digestion model in assessing the bioaccessibility of mycotoxins from food. Food and Chemical Toxicology, 43(1), 31–40. https://doi.org/10.1016/j.fct.2004.08.007
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Wang, X., You, J., Li, X., Xu, Y., Li, Z., & Wang, L. (2025). Polysaccharides: A natural solution for mycotoxin mitigation and removal. Food Chemistry, 496, 146909. https://doi.org/10.1016/j.foodchem.2025.146909
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Jun 17, 2026
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Macit, A., Sevim, S., Sancak, B. ., & Kizil, M. (2026). Impact of probiotics and β-glucan on the detoxification and gastrointestinal bioaccessibility ofaflatoxin B1 in a cereal-based fermented beverage (boza). Italian Journal of Food Science, 38(2), 321–332. https://doi.org/10.15586/ijfs.v38i2.3574
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How to Cite
Macit, A., Sevim, S., Sancak, B. ., & Kizil, M. (2026). Impact of probiotics and β-glucan on the detoxification and gastrointestinal bioaccessibility ofaflatoxin B1 in a cereal-based fermented beverage (boza). Italian Journal of Food Science, 38(2), 321–332. https://doi.org/10.15586/ijfs.v38i2.3574